Impact of Lighting on Flora and Fauna
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Technology, especially artificial light at night (ALAN), often has unexpected impacts on the environment. This chapter addresses both the perception of light by various organisms and the impact of ALAN on flora and fauna. The responses to ALAN are subdivided into the effects of light intensity, color spectra, and duration and timing of illumination. The ways organisms perceive light can be as variable as the habitats they live in. ALAN often interferes with natural light information. It is rarely neutral and has significant impacts beyond human perception. For example, UV light reflection of generative plant parts or the direction of light is used by many organisms as information for foraging, finding spawning sites, or communication. Contemporary outdoor lighting often lacks sustainable planning, even though the protection of species, habitat, and human well-being could be improved by adopting simple technical measures. The increasing use of ALAN with high intensities in the blue part of the spectrum, e.g., fluorescent light and LEDs, is discussed as a critical trend. Blue light is a major circadian signal in higher vertebrates and can substantially impact the orientation of organisms such as numerous insect species. A better understanding of how various types and sources of artificial light, and how organisms perceive ALAN, will be an important step towards more sustainable lighting. Such knowledge is the basis for sustainable lighting planning and the development of solutions to protect biodiversity from the effects of outdoor lighting. Maps that describe the rapid changes in ALAN are urgently needed. In addition, measures are required to reduce the increasing use and intensity of ALAN in more remote areas as signaling thresholds in flora and fauna at night are often close to moonlight intensity and far below streetlight levels.
KeywordsArtificial Light Spiny Mouse Volatile Organic Compound Emission Light Pollution Swimming Depth
List of Abbreviations
Artificial light at night
Brown adipose tissuelx lux
White adipose tissue
Light allows us to perceive distances, spaces, movements, and rhythms. It is pure energy – light is life. Humans differ from animals in being able to overcome the rhythms of natural light. Artificial light at night (ALAN) became an everyday tool whose absence can no longer be contemplated. It has become an asset with enormous high technology development. Today light is not only used for perceiving visual information but also to deliver data around the globe. New technological developments in the use of light will shape the human economies and production activities significantly in the future. But how much do we understand about this signaling tool we use everyday? Most humans cannot imagine living without ALAN, but at the same time, they do not realize to what extent natural nightscapes are illuminated. Our awareness rises when blackouts accidentally switch off ALAN in urban areas and the natural nightscape becomes visible. The introduction of ALAN has caused an unprecedented disruption to the transformation of nightscapes over large areas of the Earth. There have been no natural analogues, at any timescale, to the nature, extent, distribution, timing, or rate of spread of ALAN (Gaston et al. 2015). The use of ALAN increased by about 6 % annually during the last decades (Hölker et al.2010a) and ALAN continues to extend further in space, time, and intensity. Its extended use can be perceived far from outside the world, but we are only starting to understand its impact on the biosphere.
This chapter addresses both the perception of light by various organisms and the impact of ALAN on flora and fauna. All life on Earth has evolved to live in cycles of light and dark. For most organisms, their temporally differentiated niche has been promoted by highly developed senses, often including specially adapted eyesight (Hölker et al.2010a). Light receptors are highly tuned on organisms’ habitat and ecological function. A high diversity of solutions evolved to cope with the challenges posed by the different light environments, in order to exploit it most efficiently. The responses to ALAN are subdivided into the effects of light intensity, color spectra, and duration and timing of illumination within this chapter.
Light Perception and Signaling Outside Human Perception
Many organisms see the world in different light than humans do. Light, which is visible to human eyes, represents only a small part of the full spectrum of biological relevant radiation. In addition, most animals have developed distinct sensory mechanisms that perfectly cope with their temporally differentiated niche and activity pattern. For example, human vision has evolved accordingly to surviving needs for diurnal activity and is thus specialized on daylight vision but limited in perceiving low-light visual cues which are important, e.g., for nocturnal and crepuscular organisms or those inhabiting dark caves.
In vertebrates, the photoreceptive cells directly sensitive to light are classified as rods and cones. Long rods function mainly in dim light <0.001 cd and provide color-blind vision in most vertebrates. The shorter cones support vision in light intensities that are stronger than 3 cd and allow color perception. This perception results from the varying spectral sensitivities of different cone cell types to various parts of the spectrum, according to their structure and length (Kelber and Roth 2006). High light intensities at wavelengths outside cone-type sensitivities may cause the same physiological response in the photoreceptor as a dim light at the peak sensitivity level. At brightness levels from 0.001 to 3 cd, both cell types are activated for mesopic vision. Retinal ganglion cells receive the signals from cones and rods and transmit the information via long axons into the brain (Berson et al. 2002). A small percentage of retinal ganglion cells are photosensitive. Some of the retinal neurons form a circadian network, a clock to reconfigure retinal circuits for enhancing light-adapted visual function during the day- and dark-adapted rod-mediated visual function at night (McMahon et al. 2014).
The wavelengths corresponding to visible light for human perception range from about 390 nm to 700 nm. Therefore, ultraviolet (UV) light, which has shorter wavelengths, cannot be perceived by most humans. UV is, for example, necessary for the synthesis of vitamin D, but excessive exposure can cause sunburn and skin cancer. Infrared radiation (IR) can only be perceived as warmth. Conversely to human vision is the perception of the UV spectrum rather important for most birds, insects, amphibians, crustaceans, and some fish and bat species (e.g., Bennett and Cuthill 1994; Mazza et al. 2002; Winter et al. 2003). This sense can be useful for orientation, foraging, and sexual attraction; it plays a critical role for pollinators to find flowers (Johnson and Andersson 2002; Winter et al. 2003) and for birds finding fruits (Altshuler 2001; Bennett and Cuthill 1994). Interestingly, UV sensitivity is present in both diurnal and nocturnal species, e.g., in nocturnal caudata (Mège et al. 2016) and insects (Eisenbeis 2006). Not only direct UV light but also the reflection of UV light in fruits and its perception by frugivorous animals is a fine-tuned ecological interaction that supports nighttime pollination and fruit dispersal (Altshuler 2001). Hence, the ban of UV emitting outdoor lighting is a necessary and timely step toward species protection.
Direction of the Light
The information of the direction of light is used by many organisms as a visual cue in addition to discriminate brightness and color. Light polarization is invisible to most humans; it refers to the state of the light describing the proportion of waves in a beam that rotate in parallel planes to each other, or at the same rotation direction, resulting in fully, partially, or unpolarized light signals (Horváth 2014; Sabbah et al. 2005).
In nature light tends to be partially linearly polarized and thus delivers information for orientation and navigation. Dung beetles (Scarabaeus zambesianus) orientate on polarized moonlight to escape in a straight line from the dung pile avoiding competition (Dacke et al. 2003). Linear polarization of clear skylight is always perpendicular to the sun–antisun direction, and so it is used as a sun compass for navigation, as revealed for the desert ant (Cataglyphis) (Wehner and Müller 2006). This sense is also used by underwater organisms, at clear water conditions and especially at lower sun elevation, e.g., during their daily vertical migration at sunset and at sunrise (Lerner et al. 2011). Crustaceans use polarization for navigation and orientation toward food. Many of their prey species are either reflective or transparent, but they change the polarization of the light (Kleinlogel and White 2008). Cuttlefish use polarization vision to improve detection of predators in turbid conditions (Cartron et al. 2013). Water-emerging insects find their habitat mainly on horizontally polarized light reflected from the water surface (Horváth and Csabai 2014). Nonbiting midges (Chironomidae) orient on reflected polarization of the water surface to oviposit at sites with suitable food availability for their larvae (Lerner et al. 2008).
Artificial polarization is a risk for populations that depend on this signal. For example, aquatic insects attracted to highly horizontally polarizing light, such as asphalt under streetlighting, may mistakenly land or oviposit on the dry surfaces causing the fatal consequence of desiccation (Horváth et al. 2009). The lunar skylight polarization signal can be polluted by urban lighting, which indicates that nocturnal animal navigation systems, which depend on perceiving polarized moonlight, likely fail to operate properly in highly light-polluted areas (Kyba et al. 2011). Consequently, future light management should take polarization into account for species protection.
Receptors for Light
Opsins are responsible to mediating the conversion of a photon of light into an electrochemical signal. They are essential joints of communication between the internal and external environment of photoreceptor cells in prokaryotes, some algae, and animals. In plants, fungi and Placozoa, however, no opsins have yet been recorded. The great variety of opsins is classified according to the function and spectral absorption maximum. Photopsin is a superior term for photoreceptor proteins found in the cone cells of the retina that are the basis of color vision. Rhodopsin is the primary pigment found in rod photoreceptors. It is enabling vision in very low-light conditions without color discrimination (Litman and Mitchell 1996).
Cryptochromes are blue light-sensing photoreceptors found throughout the kingdom of live, in bacteria as well as in plants, animals, and humans. These flavoproteins are involved in the circadian rhythm and development of plants and animals and in some species in the sensing of magnetic fields (Lohman 2010). They absorb light associated with short, blue light wavelength spectra, not exceeding 500 nm (Ahmad and Cashmore 1996), and activate photocatalytic processes. These photobiological processes are considered as an evolutionary composition, which evolved approximately 3.5 billion years ago (Kritsky 1984).
The best-known photoreceptors of plants, fungi, and bacteria are phytochromes , a family of chromoproteins involved in circadian rhythms, growth, and development (Auldridge and Forest 2011; Chen et al. 2004; Giraud and Verméglio 2008; Rodriguez-Romero et al. 2010). Phytochromes are mainly sensitive to red and far red light (660 and 730 nm, respectively). In microbial systems, phytochrome sensitivities extend in yellow, green, blue, and violet portions of the spectrum (Rockwell and Lagarias 2010).
Carotenoid pigments are responsible for the reception of photoperiodic responses in invertebrates, such as induction of the seasonal metabolism break or migration (Veerman and Veenendaal 2003; Veerman 2001).
Another recently detected opsin, the melanopsin is involved in circadian rhythm signaling processes and pupillary reflex in retinal ganglion cells in the eyes of humans and other vertebrates (Berson et al. 2002; Hankins et al. 2008; Hattar et al. 2002; Provencio et al. 2000; Zaidi et al. 2007). The circadian rhythm signaling is mediated over the suprachiasmatic nucleus, which regulates body functions associated with the 24-h rhythm. It triggers the pineal gland, also called the “third eye,” a small endocrine gland in the epithalamus of the vertebrate brain. It is shaped like a pine cone and lies between the two halves of the thalamus. It produces melatonin, a serotonin-derived hormone, which affects the modulation of recreational patterns in both seasonal and circadian rhythms (Pévet et al. 2006). While in mammals, the pineal gland purely serves as a neuroendocrine organ, it is photoreceptive in nonmammalian vertebrates such as fish and amphibians (Ekström and Meissl 2003).
Responses to Light
Light is not neutral; it is the main source of energy for most primary producers and a major factor in controlling many physiological and behavioral processes. It is an important signal for growth, spatial movement, orientation, and communication, triggering community structure and energy flow through the food web. Responses to light are multifaceted and highly species depended. ALAN used inappropriately threats biodiversity by impacting trophic, social, and competitive interactions, masking seasonal and daily rhythms and thus altering community structure, ecosystem processes, and properties (Longcore and Rich 2004; Hölker et al.2010b; Gaston et al. 2013, 2015; Kurvers and Hölker 2014).
Responses to Light in Plants
Plants react to their light environment with stomata opening and chloroplast movement and alter their growth in response (Briggs and Christie 2002; Keller et al. 2011). Signals perceived by the phytochrome system adjust growth according to the daily and seasonal needs, e.g., photoperiodic induction of flowering, leaf senescence, and abscission. It also regulates other responses including the germination of seeds; the elongation of seedlings; the size, shape, and number of leaves; or the synthesis of chlorophyll. Plants use the phytochrome system to grow away from shade and toward light and to compare the length of dark periods (Keller et al. 2011). Physiological responses are triggered by light intensity, wavelength spectra, and duration.
Low-light conditions inhibit plant growth and development by affecting gas exchange, whereas excess light intensity has detrimental effects on the photosynthetic apparatus. As a result, plants have developed sophisticated mechanisms to adapt their structure and physiology to the prevailing light environment.
For the optimal development of, e.g., young tomato plants, a flux density of about 300 μmol m−2 s−1 photosynthetic photon, comparable to a sunny day, is recommended (Fan et al. 2013). At diffused light conditions, the need in photosynthetic photons for optimal development is decreased: This is probably due to light penetration into the lower layers of the leaf canopy, resulting in an increased CO2 fixation rate by the whole canopy (Tani et al. 2014). Diffused light condition can be achieved in greenhouses by foil and glass to save energy costs. Diffused ALAN by the atmospheric scattering, the so-called skyglow , might consequently also have a higher impact on plant responses, than direct radiation. Skyglow can lead to nighttime brightness up to thousandfold above that experienced by organisms during their evolutionary history (Kyba et al. 2015a). Although the intensity of skyglow is small compared to direct streetlight, it extends over vastly larger areas (Kyba and Hölker 2013). Surprisingly, the impact of skyglow on plants is today neither considered nor studied.
Responses in plants to wavelength are numerous. Certain spectra regulate photosynthesis, morphology, phototropism, volatile organic compound emission, and synthesis of secondary metabolites, leaf thickness, or quantity of cuticle wax (Vänninen et al. 2010).
The UV-B (280–320 nm) and the UV-A light spectrum (320–390 nm) are especially critical for plants. Low doses induce specific photomorphogenetic and developmental responses, whereas high doses result in stress signal transduction, triggering protection from damage to the photosynthetic apparatus in excess of light (Johanson et al. 1995).
The responses to the UV-A light spectrum contribute to maximizing photosynthetic potential and activated respiration in acceptable light intensities (Tsuboi and Wada 2011). The blue wavelength spectrum from 390 to 500 nm is catalytic for several metabolic and growth processes in plants, e.g., phototropism, chloroplast relocation, stem elongation, photoperiod-dependent flowering induction, resetting of the circadian oscillator, and control of stomatal opening. Strong blue light activates the incorporation of carbon in amino acids, leading to a lower amount of starch formation in leaf chloroplasts, and increases the biosynthesis of proteins (Vänninen et al. 2010). Blue light upregulates genes that encode key enzymes in the Calvin cycle, whereas green to red light spectra (500–600 nm) downregulate these genes. The phytochrome responds to red light with initiation of cell growth. Especially sodium streetlighting radiating a big ratio at 589 nm, the so-called sodium line , can stimulate phytochrome responses and plant growth (Cathey and Campbell 1975).
Not only single narrow bandwidths of spectra stimulate plant responses but rather the ratio of different spectra. The relative amount of blue to red, e.g., triggers photosynthetic activity, or the relation of red to far red is critical for seed germination, seedling establishment, shade-avoidance response, and floral induction. The green spectrum of the light (500–580 nm) tends to temper or negate the effects of blue and red light in plants (Vänninen et al. 2010).
Timing and Duration of Illumination
Light duration can induce flowering, nutrient uptake, volatile organic compound emission, and synthesis of secondary metabolites (Vänninen et al. 2010). The circadian rhythm is triggered by light and temperature. It is intensely studied with Arabidopsis mutant plants, which changed the rhythm accordingly to altered associated genes. Interestingly, the photoreceptor expression (phytochrome and cryptochrome) is itself rhythmic, indicating that the clock gates its sensitivity to light (McClung 2006). Arabidopsis clock mutants with longer periods (28 h) accumulated lower biomass than those with short periods (20 h) when grown under short cycles (10 h light/10 h dark), indicating impaired physiological function, including lower rates of chlorophyll production and carbon fixation (McClung 2006).
Plants with light-dependent flower induction have critical associated daylengths. Long-day plants induce flower buds when the days are longer than their critical daylength. In northern latitudes, these plants flower in summer. Short-day plants induce flowering when the days are shorter than their critical daylength. They flower in spring or fall in northern hemisphere. Day-neutral plants form flowers independent of the daylength. The perception of daylength in long-day Arabidopsis adjust to the phase angle of circadian rhythms relative to the light–dark cycle, rather than measure the absolute duration of light and darkness (Roden et al. 2002).
The photoperiod is a critical determinant of the oxidative stress response. Queval et al. (2007) have shown links between daylength and the rate of oxidative cell death. Defense genes and oxidative stress-responsive transcripts are induced to a greater extent in short days than in long days. Dim nocturnal light can in some species inhibit recovery from leaf damage caused by atmospheric ozone, e.g., in subterranean clover (Trifolium subterraneum) (Vollsnes et al. 2009). Since the patterns of anthropogenic light pollution and ozone pollution are spatially correlated on a global scale (Cinzano et al. 2001; Ashmore 2005), Gaston et al. (2013) demand a closer look on the extent to which low-intensity nighttime light could affect repair and recovery from ozone damage.
Responses to Light in Arthropods
“There is more mechanistic evidence for caterpillar-booms than for baby booms following power outage” (van Geffen 2015).
Moths are not only attracted to ALAN sources in great number; female moths of the orders Geometridae (inchworms) are also less active and emit less sex pheromones under ALAN conditions, resulting in reduced mating success (van Geffen et al. 2015).
Arthropods use visual cues to orient, navigate, and avoid predators or locate host plants, prey, and mates (Prokopy and Owens 1983). As many insects are attracted to light, ALAN functions like a vacuum cleaner. It is able to suck them out of their natural habitat (Eisenbeis 2006). Several theories try to explain the diversity of behaviors of insects around artificial sources of light. One reason is their navigation behavior. The optomotor system stabilizes the course by retinal images of the sky. The retinal image does not change as long as the animal moves along a straight line, when rotating the signal changes. The disturbance resulting in involuntary rotation can be corrected by compensatory body movements. The animal will rotate until it has reestablished its former retinal image (Wehner 1984; Frank 2006). Furthermore, an insect flying from artificial light into darkness or from darkness into light may be functionally blind until eye pigments have returned to their dark-adapted positions. Similar mechanisms might also be responsible for affecting both abundance and composition in aquatic arthropods such as amphipods (Navarro-Barranco and Hughes 2015).
The massive attraction of disoriented prey to ALAN sources results in predator accumulation. The bridge spider (Larinioides sclopetarius), for example, rapidly increases its reproductive activity by the periodically excessive supply of emerging water insects (Kleinteich and Schneider 2011) and is attracted to artificial lights in manmade habitats (Heiling 1999). However, the ability to benefit from prey attraction to artificial light differs between nocturnal spiders. Most orb spider species are rather sensitive to light, and some even require absolute darkness for web building, e.g., the Walnut orb-weaver spider (Nuctenea umbratica) or the silver-sided sector spider (Zygiella x-notata) (Zschokke and Herberstein 2005).
Already at light levels around moonlight (0.3 lx at maximum), many arthropods are affected. For some the threshold lies even beyond. Such light levels are already reached by urban skyglow (Kyba et al. 2015). The occurrence of species communicating with bioluminescence, e.g., fireflies (Lampyridae), rapidly decreases when a threshold of 0.5 lx is exceeded (Hagen et al. 2015). Aquatic insects in stream systems drift at nocturnal light levels below 0.001 lx to avoid predation by fish (Bishop 1969). And for water fleas (Daphnia sp.), a keystone herbivore in lakes, it has been described that even skyglow can suppress both the amplitude and the magnitude of the diel vertical migration. The reduced nocturnal upward movement into upper water layers may release phytoplankton from grazing pressure and thus may influence water quality in urban waters (Moore et al. 2000).
Both skyglow and direct light might play a role for the onset of long-distance flights of moths. For example, Riley et al. (1983) describe that the onset of “dusk flights” occurred when the irradiance level fell on average to 2.7 × 10−5 Wm−2 nm−1 in the 450–800 nm range (about 2 lx).
The spectral sensitivity in arthropods has as many facets as their habitats and ecological functions. Most insects have three different receptor types, one being sensitive to UV light with a peak sensitivity around 350 nm, another to blue light at 440 nm, and a third to green light around 540 nm (Kelber et al. 2003). In contrast, cockroaches and ants possess two photoreceptors, water fleas four, and flies and some butterflies five, or stomatopod crustaceans have evolved even twelve spectral photoreceptor types (Kelber and Roth 2006). Arthropods’ responses to color are influenced by the dominant wavelength and by the composition of wavelengths.
The broader the spectrum of the ALAN light source, the wider is the range of arthropod species that will respond to the light (Davies et al. 2013). The streetlight type attracting the most insects is the white and UV light-emitting mercury vapor light (Eisenbeis 2006). It draws seven times as many insects as comparable LED light (van Grunsven et al. 2014). The attraction of moth species to fluorescent lamps with various filters for wavelengths and radiance in the UV spectrum correlates negatively with the wavelength and positively with morphological characteristics of moth species, especially with their eye size (van Langevelde et al. 2011). LEDs are considered by some authors as relatively unattractive for insects compared to long wavelength emitting low-pressure sodium lamps (e.g., Eisenbeis and Eick 2011). In contrast, a study by Pawson and Bader (2014) demonstrates greater attraction to LEDs than to high-pressure sodium lamps irrespective of the color temperature of the LEDs. The diverse attraction to LED light is today not understood. It is most possibly related to the different radiation angle and species affinity to short wavelengths, which are emitted to a great part by LEDs.
UV light was observed to be attractive to winged aphid specimen, triggering the rising from the leaf to the sky and hence migratory behavior; instead green light attraction is related to vegetative behavior for host selection mechanism (Döring 2014). The attraction to green light was found to be altered in plant virus-infected whiteflies potentially leading to advantages in spreading the virus to other plants (Jahan et al. 2014).
The shorter wavelengths of the UV-B spectrum have adverse effects on the survival, development, egg hatchability, and fecundity. This part of the spectrum seems to be crucial for the flight activity, takeoff, and initiation of dispersal (Johansen et al. 2011). The tolerance of UV radiation is related to species and their associated habitat, and for some species living in dark habitat, e.g., fruit flies (Drosophila melanogaster), longer wavelength of the visible blue light spectrum is rather detrimental than the UV light. Hori et al. (2014) therefore consider the potential of high-intensity monochromatic blue LED radiation for species-specific economic pest control.
In future knowledge about various effects of the spectral power distribution of artificial light might be more exploited to trigger favorable processes for plant production and pest reduction in greenhouses. For example, the illumination with low-intensity violet-blue light can prevent diapausing in a beneficial insect predator (Orius insidiosus), while allowing optimal flowering in the short photoperiod host plant (Dendranthema grandiflora) of its prey (Stack and Drummond 1997). The use of LED lighting in greenhouses is of high interest to plant growers as the narrow spectrum light emission from LEDs can be matched to plant responses without wasting energy on nonproductive wavelengths (Massa et al. 2008; Stutte 2009). However, the physiological interpretation or evolutionary patterns of wavelength sensitivity in arthropods today still bear many open questions. It is, for example, not yet understood, why two phylogenetically closely related orders Trichoptera and Lepidoptera show different sensitivity patterns (van Grunsven et al. 2014).
Timing and Duration of Illumination
In arthropods like in plants, the photoperiod often acts in concert with other physical or biological background information, like temperature, moisture, humidity and cues from food, and conspecific density (Danks 2005). The responses are often triggered by hormones such as melatonin, which was found to have different circadian concentrations in various organs, possibly related to differences in melatonin function. In the hemolymph of Australian black field crickets, Teleogryllus commodus, constant illumination was linked to a low circulating melatonin concentration and a negative impact on immune parameters (Durrant et al. 2015). Female crickets (Gryllus bimaculatus) held at a 12/12 light–dark cycle expose significantly higher melatonin levels in the compound eye, brain, and palp during the dark period. Conversely, melatonin levels were significantly higher during the light period in the cercus, ovipositor, antenna, hind leg, and ovary (Itoh et al. 1995). Daily rhythms are found for many activities related to reproduction, such as the onset and length of the calling time by females, the response of males to the call, pheromone production, and release and mating activity (Saunders 2002).
The critical photoperiod for the induction or termination of diapauses or eliciting migration is species specific and often dependent on its geographical origin (Veerman 2001). Animals living in the far north are thought to have a longer critical photoperiod than animals at the equator. Van Geffen et al. (2014) found the pupation duration of the noctuid moth, Mamestra brassicae, reduced by artificial light, indicating that diapause can be inhibited by ALAN, when temperature is clement.
Responses to Light in Fish and Amphibians
Aquatic systems and their adjacent terrestrial ecosystems are very likely to be affected by changed natural light due to ALAN, because humans tend to live close to waters (Kummu et al. 2011; Perkin et al. 2011). Especially the illumination of running waters in urban environments is sometimes disproportionally higher than other natural areas such as forests, lakes, meadows, and pastures (e.g., Kuechly et al. 2012). Given the expected prevalence of light along aquatic systems, it may affect typical aquatic vertebrates such as fish and amphibians. Most amphibian species are nocturnal and many are endangered by anthropogenic stress (Hölker et al.2010b; Stuart et al. 2004). Baker and Richardson (2006) demonstrate that green frogs (Rana clamitans melanota) produce fewer advertisement calls and move more frequently under streetlighting than under ambient light conditions. The study clearly shows that male frog behavior is affected by the presence of ALAN in a manner that has the potential to affect population dynamics.
Also fish species are affected by ALAN. Artificial light is used worldwide in fisheries to attract fish, squid, and other marine food (Davies et al. 2014). Several fish species behavior including the hatching process is light dependent (McAlary and McFarland 1993). Thus, ALAN has a great potential to interfere with the circadian behavior of aquatic organisms (Perkin et al. 2011; Davies et al. 2014).
The physiological and behavioral responses of many fish can be triggered at very low light levels, below 1 lx, which may make even the light levels produced by skyglow an ecologically relevant light source. Such low light levels have been shown to be an important cue for both predator avoidance and feeding, for example, in salmoniformes. ALAN at 1 lx can delay the dispersal timing of Atlantic salmon (Salmo salar) fry by up to 2 days and extend the dispersal period into daylight hours (Riley et al. 2015). The period between fry dispersal and the establishment of feeding territories is of critical importance in the dynamics of salmonid populations, and any disruption may significantly increase predation and reduce fitness. In caged Atlantic salmon (Salmo salar), the swimming depth could be adjusted by artificial lighting (Juell and Fosseidengen 2004). Salmon groups swam deeper and at lower density, both day and night, in cages illuminated by lamps at different depths. When underwater lamps were lowered from 1 to 15 m and subsequently raised again during a period of 48 h, swimming depth correlated with lamp depth.
Brüning et al. (2015) showed nocturnal suppression of melatonin and suppressed gene expression of gonadotropins (Brüning et al. 2016) in European perch (Perca fluviatilis) at 1 lx. However, cortisol levels were not affected by the tested light intensities, indicating rather hormonal response than a stressful disturbance by the light (Brüning et al. 2015).
Streetlight and especially illumination of bridges might potentially interfere with migratory behavior of certain fish species, resulting in excessive energy loss and spatial impediments to migration, which in turn can result in reduced migratory success (Hölker et al.2010b). For example, flume experiments demonstrate a strong avoidance reaction of silver eels (Anguilla anguilla) to ALAN (Hadderingh et al. 1999), and streetlighting delays and disrupts the dispersal of Atlantic salmon (Salmo salar) fry (Riley et al. 2015).
Anuran activity in natural habitats under nocturnal conditions has been found down to 0.00001 lx (Buchanan 2006). Slight increases in illumination caused by nearby lights or even by skyglow may alter foraging behavior or antipredator response of frogs (Buchanan 2006; Baker and Richardson 2006). Red-backed salamanders (Plethodon cinereus) orient toward prey sooner at higher ambient illuminations (0.001 lx) compared to lower light levels indicating improved visually based foraging ability at higher light levels (Perry et al. 2008). However, fewer salamanders were active in lighted transects (0.01 lx) compared to unlighted transects.
Frogs typically exhibit phototaxis and move toward blue light (less than 500 nm) at intensities higher than ambient illumination (Buchanan 2006). However, strong interaction effects between intensity and wavelength preference are observed, making it difficult to predict the behavior of frogs. Thus, more field studies of intensity-dependent and spectrally dependent phototaxis are needed. Most frogs studied have trichromatic color vision and possibly tetrachromatic color vision with sensitivity in the ultraviolet wavelengths (Buchanan 2006).
The natural light spectra in water depend on the composition of the water. In seawater only mid-wavelengths such as blue-green (450–550 nm) are reaching deeper parts, whereas in shallow waters a broader spectrum with short (UV) or long (red) wavelength can be present (Myrberg and Fuiman 2002). In most lakes, however, yellow light penetrates the water the deepest (Lythgoe 1988). Shallow water organisms have broad spectral sensitivities. With depth the sensitivity of water organisms alters toward middle wavelengths (Cronin et al. 2010). Animals that live in different water depths may perceive color throughout almost the entire spectral range of available light. In species, which change their habitat depending on their size, the vision perception can change with their developmental stage (Boeuf and Le Bail 1999). Findings in fishes of the upper part of the water column indicate great sensitivity of the pineal or other nonvisual photoreceptors to blue light (e.g., Vera et al. 2010). Brüning et al. (2016) found that all colors (blue, green, and red) suppressed melatonin production in perch. They describe blue light as less effective for melatonin suppression, which corresponds to the different light conditions in perch habitats.
UV and red fluorescent light serves species recognition and short distance communication in coral reef inhabiting fish with the benefit that many predatory fish are unable to detect the wavelengths (Gerlach et al. 2014). Red fluorescence is particularly well suited for short-range visual interactions in reef fish as its information content is rapidly lost at greater distances and thus not detectable for most predators. For example, the fluorescent color pattern of Cirrhilabrus solorensis peaks at around 660 nm, a visual range for which most reef fish inhabiting depths below 10 m have poor or no sensitivity.
Timing and Duration of Illumination
Fish species are either more active in light, less active in darkness, or vice versa. The photoperiod is important in synchronizing locomotor activity rhythms and food intake (Boeuf and Le Bail 1999). Photoperiod affects reproduction in fish. It is considered the most important environmental cue for breeding seasonality and maturation. In aquaculture, the manipulation of photoperiod is an efficient tool to induce reproductive events. It is used to induce, e.g., reproductive maturation and egg ovulation outside of natural spawning periods (Kolkovski and Dabrowski 1998; MacQuarrie et al. 1979). In natural environments, ALAN might cause similar effects or problems such as disturbance of synchronous hatching and swim bladder inflation of fish larvae, reducing survival chances (Riley et al. 2015; Brüning et al. 2011).
For amphibians the daylength is one of the most important factors to predict seasonal changes in their environment. The trigger is required to anticipate the future changes in their thermal environment for bio-thermal adaptation (Sanabria and Quiroga 2011) and behavioral synchronization (Canavero and Arim 2009). For many fish and amphibians, rapid changes in light levels at night (e.g., by vehicle headlights) can lead to a massive loss of visual information. The periods of light and dark adaptation in juvenile pacific salmon and several nocturnal frogs can be more than 1 h (Buchanan 2006; Nightingale et al. 2006). During these transition periods, organisms are temporarily “blind” for their visual environment.
Responses to Light in Birds and Reptiles
Birds and reptiles perceive light even in the absence of input from the eyes or associated neurotransmitters. Recently, Fulgione et al. (2014) found opsins at the skin of the belly of the moorish gecko (Tarentola mauritanica), which perceive ambient color and initiate camouflage color changing of the skin without the input via the eye.
Magnetoreception is another necessary tool for birds and reptiles to navigate. The signaling is a complex system, involving interactions between magnetoreceptors and visual cues. Artificial light might interfere with these highly species-specific developed senses which are not yet fully understood (Wiltschko et al. 2009).
The extension of the individual daylength in birds due to ALAN is today well known. Male birds probably start singing at dawn when stimulation by increasing light intensities has reached a certain threshold level. This threshold varies among species, leading to species-specific timing of dawn song. Along an urban gradient ranging from an urban forest to the city center, the onset of blackbird (Turdus merula) dawn song differs up to 5 h (Nordt and Klenke 2013). The period of onset of singing before dawn increases with light intensity by 1.5–2 min per lux (Da Silva et al. 2014). Streetlighting affects the timing of dawn song, the strongest in species that under natural conditions start singing early, e.g., the blackbird or robin (Erithacus rubecula), and is neglectable in species that naturally initiate singing late, e.g., the chaffinch (Fringilla coelebs) (Kempenaers et al. 2010). The rooster crowing can also be induced with light stimulation using intensities of 1 lx for 30 min at dawn, and the number of crows can be increased with lighting intensity (Shimmura and Yoshimura 2013). In an experiment, artificial lighting at 1.6 lx caused great tits (Parus major) to wake up earlier, sleep less (−5 %), and spend less time in the nest box as they left their nest box earlier in the morning. Females spent a greater proportion of the night awake (Raap et al. 2015). De Jong et al. (2016) found that the increased activity is not limited to a certain threshold but occurs even when nocturnal light levels are slightly increased.
Being ectothermic, reptiles cannot tolerate cold climates in most cases and thus are mainly adapted to diurnal conditions and bright sunlight. Some clades associated with warm climate, such as geckos, show strong tendencies toward nocturnal activity (Perry and Fisher 2006). Sea turtles may be disorientated even by skyglow to the extent that their migration habits are affected (Salmon 2006). They orient on the reflection of starlit water surface to rapidly enter their habitat after hatching at beaches.
In the common lizard (Zootoca vivipara), Martin et al. (2015) found extended spectral sensitivity in the UV spectrum and the near infrared, which is a rare feature in terrestrial vertebrates. It enables discrimination of small differences in throat coloration and might have coevolved with the visual communication system.
Migrating bird species get attracted by the visible red light, the spectrum between 680 and 550 nm, or UV light. Poot et al. (2008), therefore, discuss the reduction of fatal injuries of migrating birds associated with ALAN by using light of the green and blue spectrum. It offers the highest sensitivity for human night vision but is outside the cone sensitivity of birds. However, Ogden (1996) debates that birds perceive color throughout the spectrum and that rather intensity than color matters. Ouyang et al. (2015) found that adult great tits nesting in white-light transects had higher corticosterone concentrations than individuals nesting in green light or dark control. Individuals in red light had higher corticosterone levels when they nested closer to the lamppost than individuals nesting farther away, a decline not observed in the green or dark treatment. This is fitness relevant because individuals with high corticosterone levels had fewer fledglings.
Timing and Duration of Illumination
The simplest solution to reduce fatal accidents with nighttime migratory bird is to turn off light, especially after midnight, when birds begin to descend from their peak migration altitude. The peak migratory periods are in spring and autumn (Krijgsveld et al. 2015); it seems to be a reasonable timing to turn off hazardous lighting for migratory birds after midnight. Where it is not possible to turn off the light, shielding can direct light downward. This is also an effective measure for many other species, e.g., for marine turtle protection to reduce disruption of visual cues for orientation at the nesting beach.
In urban agglomeration, ALAN interferes with the circadian rhythm of birds and suppresses melatonin even at low light levels (de Jong et al. 2016). Earlier dawn singing in the season is known for blackbirds (Turdus merula), robins (Erithacus rubecula), and great tits (Parus major), whereas blue tits (Parus caeruleus) start their dusk singing earlier (Da Silva et al. 2014). The song thrush (Turdus philomelos) males, conversely, are more likely to sing at dawn earlier in the season in naturally dark sites, compared to light-polluted sites. Short winter days may be perceived by the birds as longer spring days and cause males to sing earlier in the season provided weather conditions are clement. Birds living in the city center are exposed to a subjective daylength on average 50 min longer than conspecifics breeding in a nearby rural forest (Dominoni and Partecke 2015). The difference in subjective daylength between urban and rural birds is stronger in the beginning of the breeding season, being over 1 h in March, whereas in May the difference is reduced to 6 min.
Also the seasonal period is extended by ALAN. Urban blackbirds develop a functional reproductive system 19 days in advance of their forest counterparts. ALAN affects the timing of egg laying (Kempenaers et al. 2010) and advances of gonadal growth and testosterone production by up to 1 month. This seasonal advantage for urban birds might turn to the reverse, when weather conditions inhibit food availability (Dominoni et al. 2013).
In reptiles a circadian entrainment to photoperiod was as well observed for hatching synchronization of the species Anolis sagrei (Nash et al. 2015). Hatching times of the singly laid lizard eggs are synchronized in the morning at dawn. Most males hatch after the females. The impact of ALAN on this synchronization is presently unknown.
Responses to Light in Mammals
Eutherian mammals escaped the predominant diurnal predator activity in the Mesozoic era, also called the age of reptiles, in developing visual and nonvisual systems of photoreception, which are characteristic for nocturnal lifestyle (Gerkema et al. 2013). Hence, the predation pressure is considered to be the main evolutionary driver for nocturnal vision in mammals (Jacobs 2009). Hölker et al. (2010) discuss that this important evolutionary step is currently threatened by the unforeseen implications of the widespread use of artificial light. Most mammals have nocturnal, crepuscular, or arrhythmic activity patterns. Exceptions are some rodents, squirrels, and primates including humans, which are predominately diurnal and have adopted their visual senses to daylight.
Most nocturnal mammals have few cones, e.g., bats and armadillos. These can easily become saturated by light intensities above 120 cd m−2 (light level at twilight), and the animals become temporarily blinded by brighter light exposure (Beier 2006).
Some, especially fast-flying bat species, benefit from artificial light sources due to improved foraging conditions. However, slow-flying species emerge later and appear to have an innate intolerance of lit conditions, even at relatively low light levels (Stone et al. 2015a). Light that spills on commuting routes or flyways can even cause avoidance behavior of some species. The illumination of roosts or the entrance to it can cause the bats to abandon roosts in the worst case (Stone et al.2015b). Hale et al. (2015) observed that a common urban bat (Pipistrellus pipistrellus) select dark crossing roots at gaps (e.g., at a streets) in urban tree networks and that the success to cross depends on light intensity and width of the habitat gap.
The suppression of plasma melatonin in mammals can be affected at very low light levels and sensitivities are highly species dependent. The light intensity during the photophase is important to trigger the scotophase melatonin response. In general, nocturnally active species are rated as more sensitive to ALAN, in terms of melatonin suppression, than diurnally active animals (Reiter et al. 2011). For example, diurnally active rodents require irradiances in the order of 1.85 μW cm−2 (about 13 lx), whereas in nocturnal rodents irradiances of 0.005 μW cm−2 (about 0.03 lx) are sufficient for complete melatonin suppression (Deveson et al. 2000). Also animal groups with similar circadian rhythms can differ in their sensitivities to suppress melatonin. Goats, for example, are less sensitive to ALAN than sheep (Deveson et al. 2000).
The circadian response to light in higher vertebrates, including humans, is triggered by blue light. Wavelengths around 480 nm are most effective. At this wavelength, the sensitivity is double compared to the one of green light spectrum around 555 nm. This circadian signal is not related to visual sensitivity but perceived by melanopsin photoreceptors (Brainard et al. 2001).
The basically nocturnal nature of mammals may have led to predominately dichromatic vision (Jacobs 2009). Primates developed the additional ability to sense red color. This trichromatic vision is discussed to optimize food finding in frugivorous animals (Vorobyev 2004). In some species, females developed trichromatic vision, whereas male vision stays dichromatic (Jacobs 1994).
UV vision in mammals is discussed as restricted to rodents and marsupials. However, a study on evolutionary history of 33 bat species spanning 65 million years discovered a more important role for UV vision than previously estimated (Zhao et al. 2009). Seven insectivorous species of bats, representing five genera and three families, were recently found to be sensitive to dim-light UV vision (Gorresen et al. 2015). The European mole (Talpa europaea) is mainly adapted to underground life and thus the anatomy of its visual system is subjected to an involution. However, the mole was recently found to perceive colors and to be sensitive in the UV spectrum (Glösmann et al. 2008).
Timing and Duration of Illumination
Reproduction of mammals living in temperate regions follows seasonality to ensure the birth of offspring in spring or summer, when optimal survival conditions are given. Species with a short incubation or gestation period such as hamsters and species with a circannual gestation period such as horses are long-day breeders, and their fertile period occurs in the springtime. Species with a gestation period around 5–6 months such as sheep and goats are short-day breeders and their breeding takes place in autumn. The pineal hormone melatonin is the common link between photoperiod and reproduction (Gerlach and Aurich 2000). The reproductive state is not determined by the absolute daylength but by the direction of change. Rams exposed to alterations of short and long days at 1-month intervals maintain a continuously high testicular activity (Gerlach and Aurich 2000).
In order to adopt to seasonal changes, the night-active mouse lemurs (Microcebus murinus) turn less active and cease eating when exposed to ALAN, compared to simulated moonlight treatment. The core temperatures, during night and the day resting time, are significantly higher under exposure to ALAN, in order to acclimatize to long-day photoperiod (Le Tallec et al. 2013). Altered behavior of two spiny mouse congeners exposed to ALAN differs in chronotype. The nocturnal common spiny mouse (Acomys cahirinus) decreases activity and foraging with ALAN. Probably due to increased predation risk, it restricts movement particularly in exposed microhabitats. The diurnal mouse neither expands its activity into the illuminated hours, leading to reduced overall activity and a relatively underexploited temporal niche, which may promote invasion of alien species that are less light sensitive (Rotics et al. 2011).
In different studies on mammals, there is convincing evidence that extended light exposure causes weight gain, even when calorie intake and physical activity are held constant (e.g., Fonken et al. 2013; Salgado-Delgado et al. 2010). When mammals escaped the diurnal predation pressure and conquered the nocturnal niche, they had to develop mechanisms to protect from low temperature at nighttime. Brown adipose tissue (BAT) is exclusively found in mammals. Its primary function is to produce heat to adapt to ambient temperature changes and to maintain the balance between energy intake and energy expenditure by means of disposing the extra energy as heat. White adipose tissue (WAT) acts as an energy storage and cold acclimation in rodents has been shown to induce a transdifferentiation from WAT to BAT (Tam et al. 2012). Melatonin supplementation to small mammals promotes recruitment of BAT, thus increases the thermogenic capacity and activity. The suppression of melatonin due to exposure to ALAN after the onset of darkness is therefore discussed to lead to body weight gain and adipose storage both in human and other mammals (Tan et al. 2011).
Melatonin further acts on the immune system as stimulant, providing a pre-activated state for a more effective early immune response against external stressors (Carrillo-Vico et al. 2013). The review links melatonin to immune system stimulation against infections (bacteria, viruses, and parasites) and against autoimmunity (multiple sclerosis, rheumatoid arthritis, type 1 diabetes, etc.), for increased antibody titers after vaccination, for preventing organ rejection after transplantation, and for an altered immune response in senescent rodents. The chronic suppression of melatonin after the onset of darkness might come along with further medical costs, which urgently need to be considered when, e.g., reasoning shift works with efficiency for the gross national product.
The introduction of artificial light has caused an unprecedented transformation of nocturnal landscapes over large areas of the Earth (Kyba and Hölker 2013). However, the emission of light is rarely neutral and may have serious ecological and evolutionary implications for many organisms, from bacteria to mammals, and may reshape entire ecosystems (Kyba and Hölker 2013). The emitted signal of ALAN is in most cases underestimated and is not yet considered as a major pollutant, but the breadth of biological impacts of ALAN provides strong evidence that ALAN can be considered as one major stressor for organisms similar to noise, soil, water, and air pollution. The question arises if ALAN impacts entire nightscapes, then to what extent is it connected to biodiversity loss worldwide. Furthermore, the increasing use of illumination technology that emits a great part in the blue spectrum, e.g., fluorescent light and LED, is a rather critical trend. Blue light is a major circadian signal for higher vertebrates (including humans) and can substantially impact insect orientation.
In order to reduce the various effects on single species and thus cascading effects in communities and ecosystems, or on ALAN-induced fragmentation of habitats, it is necessary to consider all possible measures to identify ways in which practical steps can be taken to reduce environmental concerns (Schroer and Hölker 2014). Accordingly, ALAN needs to be directed to where it is needed, only used when necessary and in the lowest intensity required for its use. For example, the illumination of historical sites could be beautiful and of great benefit to humans, but at times when humans are sleeping, the lighting of sites is rather inadequate. An over-illumination of sites could result in glare and the benefits of illumination might be reversed. When illuminating walls and natural rocks, inhabited by endangered species, the environmental impact needs to be considered besides the costs for energy consumption. During migrating periods of ALAN-sensitive fish or at times when insects like mayflies emerge in large quantities, the illumination of bridges should be reduced. In addition, the installation of artificial lights close to seminatural spaces such as green or blue urban areas should be avoided whenever possible and as far as the security and safety requirements will allow this. For the protection of biodiversity, natural darkness reserves are important, as well as the development of corridors to connect habitats of nocturnal species that avoid lit conditions. Reducing light pollution will reduce the necessary distance of urban estates to natural dark sky preserves (Aubé 2015).
Future research on the environmental effects of ALAN is critically important to understand the influence of ALAN and how to use innovative lighting technologies in order to mitigate negative consequences for humans and nature.
To what extent does the disruption of natural light regimes by ALAN influence populations, communities, and ecosystems? Of concern is not only direct illumination but also skyglow and how the two interact.
At which thresholds of light intensity and duration does artificial lighting become light pollution with a significant and relevant ecological impact, and how do these thresholds depend on spectral composition?
What size of “dark refuges”, where the intensity and/or duration of artificial light fall below such thresholds, is necessary to maintain natural ecosystem processes?
What technologies and alternative lighting strategies can address the environmental disadvantages of current lighting practices in different natural areas or settlement types?
Outdoor illumination occurs predominantly with streetlighting, airports, sea ports, industrial areas, stadiums, and public service areas (Kuechly et al. 2012; Kyba et al. 2015). In most countries, streetlighting is based on international accepted levels (e.g., CIE 115 2010); for an overview see also Kyba et al. (2014). Brightness levels produced in rural and seminatural areas on country roads, cycle and footpaths can easily reach light levels that disturb many organisms, which are active at night. Furthermore, as the growth of cities and the development of lighting technologies continue, ALAN is increasingly modifying natural light regimes by encroaching on dark refuges in space, in time, and across wavelengths (Aubrecht et al. 2010).
Cathey and Campbell (1975) suggest for the well-being of plants to shut off streetlamps 2–4 h during the early part of the evening. This timing unfortunately conflicts with safety and security issues. But, with the knowledge of species-specific action spectra and considering the rapid introduction of new lighting systems, there is today a great opportunity to adjust ALAN in order to reduce any negative environmental impacts (Gaston et al. 2015). A first step into this direction is the development of indices to distinguish the impact of ALAN on, e.g., photosynthesis, melatonin suppression, or star visibility (e.g., Aubé et al. 2013). Furthermore, the labeling of lighting products for consumer information and awareness requires urgent investigations.
Often street and public places are better illuminated than our living rooms. Future research toward the development of sustainable illumination should allow us to better balance human requirements for lit spaces with the environmental needs for unlit spaces. The goal should be to provide the light needed for any given task while minimizing both the energy use and negative environmental side effects of the light (Kyba et al. 2014).
Last but not least, maps that describe the rapid changes in ALAN are urgently needed. By developing high-resolution maps of artificial light, it will be possible to analyze the degree to which different land uses are responsible for local light pollution, which is of particular interest for conservation management (Aubrecht et al. 2008; Kuechly et al. 2012). For example, the world atlas of artificial light sky brightness (Cinzano et al. 2001) allows to determine areas of good and bad lighting and to establish and protect refuges for ALAN-sensitive organisms.
The rising of public awareness of the broad range of practices and impacts is an important step, in order to reduce negative consequences for humans and nature by the implementation of advanced lighting technologies. The recently significant increase in public involvement in light pollution research goes into this direction (e.g., http://lossofthenight.blogspot.de, http://www.stars4all.eu, http://tatortgewasser.de, http://www.citiesatnight.org) and has proven that citizen scientists provide valuable research data, for example, for monitoring global night sky luminance (Kyba et al. 2013).
We want to acknowledge the support by the European Cooperation in Science and Technology (COST) through the Action ES1204 LoNNe (Loss of the Night Network) and the national support by both the German Federal Ministry of Research and Technology (support code: 033L038A) and the Federal Agency for Nature Conservation (support code: 3514821700).
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